Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Melatonin having Therapeutic Bone Regenerating Capacity in Biomaterials

Author(s): Jinming Huang, Yi Li and Chengqi He*

Volume 23, Issue 5, 2022

Published on: 09 July, 2021

Page: [707 - 718] Pages: 12

DOI: 10.2174/1389201022666210709145347

Price: $65

Abstract

Abstract: Bone defects are usually treated with bone grafting. Several synthetic biomaterials have emerged to replace autologous and allogeneic bone grafts, but there are still shortcomings in bone regeneration. Melatonin has demonstrated a beneficial effect on bone metabolism with the potential to treat fractures, bone defects and osteoporosis. The hormone has been found to promote osteogenesis, inhibit osteoclastogenesis, stimulate angiogenesis and reduce peri-implantitis around the graft. Recently, a growing number of studies have shown beneficial effects of melatonin to treat bone defects. However, cellular and molecular mechanisms involved in bone healing are still poorly understood. In this review, we recapitulate the potential mechanisms of melatonin, providing a new horizon to the clinical treatment of bone defects.

Keywords: Melatonin, osteogenesis, bone defects, bone tissue engineering, allogeneic bone grafts, bone metabolism.

« Previous Next »
Graphical Abstract

[1]
Winkler, T.; Sass, F.A.; Duda, G.N.; Schmidt-Bleek, K. A review of biomaterials in bone defect healing, remaining shortcomings and future opportunities for bone tissue engineering: The unsolved challenge. Bone Joint Res., 2018, 7(3), 232-243.
[http://dx.doi.org/10.1302/2046-3758.73.BJR-2017-0270.R1] [PMID: 29922441]
[2]
Bahney, C.S.; Zondervan, R.L.; Allison, P.; Theologis, A.; Ashley, J.W.; Ahn, J.; Miclau, T.; Marcucio, R.S.; Hankenson, K.D. Cellular biology of fracture healing. J. Orthop. Res., 2019, 37(1), 35-50.
[http://dx.doi.org/10.1002/jor.24170] [PMID: 30370699]
[3]
Claes, L.; Recknagel, S.; Ignatius, A. Fracture healing under healthy and inflammatory conditions. Nat. Rev. Rheumatol., 2012, 8(3), 133-143.
[http://dx.doi.org/10.1038/nrrheum.2012.1] [PMID: 22293759]
[4]
Hak, D.J.; Fitzpatrick, D.; Bishop, J.A.; Marsh, J.L.; Tilp, S.; Schnettler, R.; Simpson, H.; Alt, V. Delayed union and nonunions: Epidemiology, clinical issues, and financial aspects. Injury, 2014, 45(Suppl. 2), S3-S7.
[http://dx.doi.org/10.1016/j.injury.2014.04.002] [PMID: 24857025]
[5]
Dimitriou, R.; Jones, E.; McGonagle, D.; Giannoudis, P.V. Bone regeneration: Current concepts and future directions. BMC Med., 2011, 9(66), 66.
[http://dx.doi.org/10.1186/1741-7015-9-66] [PMID: 21627784]
[6]
Gomez-Barrena, E.; Rosset, P.; Lozano, D.; Stanovici, J.; Ermthaller, C.; Gerbhard, F. Bone fracture healing: Cell therapy in delayed unions and nonunions. Bone, 2015, 70, 93-101.
[7]
Narres, M.; Kvitkina, T.; Claessen, H.; Droste, S.; Schuster, B.; Morbach, S.; Rümenapf, G.; Van Acker, K.; Icks, A. Incidence of lower extremity amputations in the diabetic compared with the non-diabetic population: A systematic review. PLoS One, 2017, 12(8)e0182081
[http://dx.doi.org/10.1371/journal.pone.0182081] [PMID: 28846690]
[8]
Kroeger, K.; Berg, C.; Santosa, F.; Malyar, N.; Reinecke, H. Lower limb amputation in Germany: An analysis of data from the german Federal Statistical Office wetween 2005 and 2014. Dtsch. Arztebl. Int., 2017, 114(8), 130.
[http://dx.doi.org/10.3238/arztebl.2017.0130]
[9]
Malyar, N.M.; Freisinger, E.; Meyborg, M.; Lüders, F.; Gebauer, K.; Reinecke, H.; Lawall, H. Amputations and mortality in in-hospital treated patients with peripheral artery disease and diabetic foot syndrome. J. Diabetes Complications, 2016, 30(6), 1117-1122.
[http://dx.doi.org/10.1016/j.jdiacomp.2016.03.033] [PMID: 27118161]
[10]
Parisi, M.C.R.; Neto, A.M.; Menezes, F.H.; Gomes, M.B.; Teixeira, R.M.; Paulo De Oliveira, J.E.; Dantas Pereira, J.R.; Chaves Fonseca, R.M.; Arruda Guedes, L.B.; Costa, E.; Forti, A.; De Oliveira, A.M.; de Nobrega, M.B.; Colares, Q.V.N.; Schmid, H.; Nienov, O.H.; Nery, M.; Fernandes, T.D.; Pedrosa, H.C.; De Oliveira, S.C.D.S.; Ronsoni, M.; Rezende, K.F.; Quilici, V.M.T.; Vieira, F.A.E.; De Macedo, C.G.M.; Stuchi-Perez, E.G.; Dinhane, I.K.G.; Pace, A.E.; De Freitas, F.M.C.; Calsolari, M.R.; Saad, A.M.J. Baseline characteristics and risk factors for ulcer, amputation and severe neuropathy in diabetic foot at risk: the BRAZUPA study. Diabetol. Metab. Syndr., 2016, 8, 25.
[11]
Wang, W.; Yeung, K.W.K. Bone grafts and biomaterials substitutes for bone defect repair: A review. Bioact. Mater., 2017, 2(4), 224-247.
[http://dx.doi.org/10.1016/j.bioactmat.2017.05.007] [PMID: 29744432]
[12]
García-Gareta, E.; Coathup, M.J.; Blunn, G.W. Osteoinduction of bone grafting materials for bone repair and regeneration. Bone, 2015, 81, 112-121.
[http://dx.doi.org/10.1016/j.bone.2015.07.007] [PMID: 26163110]
[13]
Martin, V.; Bettencourt, A. Bone regeneration: Biomaterials as local delivery systems with improved osteoinductive properties. Mater. Sci. Eng. C, 2018, 82, 363-371.
[http://dx.doi.org/10.1016/j.msec.2017.04.038] [PMID: 29025670]
[14]
Ossipov, D.A. Bisphosphonate-modified biomaterials for drug delivery and bone tissue engineering. Expert Opin. Drug Deliv., 2015, 12(9), 1443-1458.
[http://dx.doi.org/10.1517/17425247.2015.1021679] [PMID: 25739860]
[15]
Cui, Y.; Zhu, T.; Li, D.; Li, Z.; Leng, Y.; Ji, X.; Liu, H.; Wu, D.; Ding, J. Bisphosphonate-functionalized scaffolds for enhanced bone regeneration. Adv. Healthc. Mater., 2019, 8(23)e1901073
[http://dx.doi.org/10.1002/adhm.201901073] [PMID: 31693315]
[16]
Cole, LE; Vargo-Gogola, T; Roeder, RK Targeted delivery to bone and mineral deposits using bisphosphonate ligands. dv Drug Deliver Rev. 2016, 99(A), 12-27.
[17]
Reyes, C.; Hitz, M.; Prieto-Alhambra, D.; Abrahamsen, B. Risks and benefits of bisphosphonate therapies. J. Cell. Biochem., 2016, 117(1), 20-28.
[http://dx.doi.org/10.1002/jcb.25266] [PMID: 26096687]
[18]
Almeida, M.; Laurent, M.R.; Dubois, V.; Claessens, F.; O’Brien, C.A.; Bouillon, R.; Vanderschueren, D.; Manolagas, S.C. Estrogens and androgens IN skeletal physiology AND pathophysiology. Physiol. Rev., 2017, 97(1), 135-187.
[http://dx.doi.org/10.1152/physrev.00033.2015] [PMID: 27807202]
[19]
Shi, L.F.; Wu, Y.; Li, C.Y. Hormone therapy and risk of ovarian cancer in postmenopausal women: A systematic review and meta-analysis. Menopause, 2016, 23(4), 417-424.
[http://dx.doi.org/10.1097/GME.0000000000000550] [PMID: 26506499]
[20]
The NAMS 2017 hormone therapy position statement advisory panel. Menopause, 2017, 24(7), 728-753.
[http://dx.doi.org/10.1097/GME.0000000000000921] [PMID: 28650869]
[21]
Li, Y.; Bai, Y.; Pan, J.; Wang, H.; Li, H.; Xu, X.; Fu, X.; Shi, R.; Luo, Z.; Li, Y.; Li, Q.; Fuh, J.Y.H.; Wei, S. A hybrid 3D-printed aspirin-laden liposome composite scaffold for bone tissue engineering. J. Mater. Chem. B Mater. Biol. Med., 2019, 7(4), 619-629.
[http://dx.doi.org/10.1039/C8TB02756K] [PMID: 32254795]
[22]
Chin, K.Y. A review on the relationship between aspirin and bone health. J. Osteoporos., 2017, 2017(3710959)3710959
[http://dx.doi.org/10.1155/2017/3710959] [PMID: 28163951]
[23]
Zheng, S.L.; Roddick, A.J. Association of Aspirin Use for Primary Prevention with cardiovascular events and bleeding events: a systematic review and meta-analysis. JAMA, 2019, 321(3), 277-287.
[http://dx.doi.org/10.1001/jama.2018.20578] [PMID: 30667501]
[24]
Visser, R.; Rico-Llanos, G.A.; Pulkkinen, H.; Becerra, J. Peptides for bone tissue engineering. J. Control. Release, 2016, 244, 122-135.
[http://dx.doi.org/10.1016/j.jconrel.2016.10.024]
[25]
De Witte, T.M.; Fratila-Apachitei, L.E.; Zadpoor, A.A.; Peppas, N.A. Bone tissue engineering in via growth factor delivery: from scaffolds to complex matrices. Regen. Biomater., 2018, 5(4), 197-211.
[http://dx.doi.org/10.1093/rb/rby013] [PMID: 30094059]
[26]
Zhang, K.; Lin, S.; Feng, Q.; Dong, C.; Yang, Y.; Li, G.; Bian, L. Nanocomposite hydrogels stabilized by self-assembled multivalent bisphosphonate-magnesium nanoparticles mediate sustained release of magnesium ion and promote in-situ bone regeneration. Acta Biomater., 2017, 64, 389-400.
[http://dx.doi.org/10.1016/j.actbio.2017.09.039] [PMID: 28963020]
[27]
Okuzu, Y.; Fujibayashi, S.; Yamaguchi, S.; Yamamoto, K.; Shimizu, T.; Sono, T.; Goto, K.; Otsuki, B.; Matsushita, T.; Kokubo, T.; Matsuda, S. Strontium and magnesium ions released from bioactive titanium metal promote early bone bonding in a rabbit implant model. Acta Biomater., 2017, 63, 383-392.
[http://dx.doi.org/10.1016/j.actbio.2017.09.019] [PMID: 28919512]
[28]
Case, J.D.; Takahashi, Y.; Lee, T.H.; Mori, W. Isolation of melatonin, the pineal gland factor that lightens melanocytes. J. Am. Chem. Soc., 1958, 80(10), 2587-2587.
[http://dx.doi.org/10.1021/ja01543a060]
[29]
Venegas, C.; García, J.A.; Escames, G.; Ortiz, F.; López, A.; Doerrier, C.; García-Corzo, L.; López, L.C.; Reiter, R.J.; Acuña-Castroviejo, D. Extrapineal melatonin: analysis of its subcellular distribution and daily fluctuations. J. Pineal Res., 2012, 52(2), 217-227.
[http://dx.doi.org/10.1111/j.1600-079X.2011.00931.x] [PMID: 21884551]
[30]
Conti, A.; Conconi, S.; Hertens, E.; Skwarlo-Sonta, K.; Markowska, M.; Maestroni, J.M. Evidence for melatonin synthesis in mouse and human bone marrow cells. J. Pineal Res., 2000, 28(4), 193-202.
[http://dx.doi.org/10.1034/j.1600-079X.2000.280401.x] [PMID: 10831154]
[31]
Amstrup, A.K.; Sikjaer, T.; Mosekilde, L.; Rejnmark, L. Melatonin and the skeleton. Osteoporos. Int., 2013, 24(12), 2919-2927.
[http://dx.doi.org/10.1007/s00198-013-2404-8] [PMID: 23716040]
[32]
Poeggeler, B.; Reiter, R.J.; Tan, D.X.; Chen, L.D.; Manchester, L.C. Melatonin, hydroxyl radical-mediated oxidative damage, and aging: a hypothesis. J. Pineal Res., 1993, 14(4), 151-168.
[http://dx.doi.org/10.1111/j.1600-079X.1993.tb00498.x] [PMID: 8102180]
[33]
Manchester, L.C.; Coto-Montes, A.; Boga, J.A.; Andersen, L.P.H.; Zhou, Z.; Galano, A.; Vriend, J.; Tan, D.X.; Reiter, R.J. Melatonin: an ancient molecule that makes oxygen metabolically tolerable. J. Pineal Res., 2015, 59(4), 403-419.
[http://dx.doi.org/10.1111/jpi.12267] [PMID: 26272235]
[34]
Reiter, R.J.; Mayo, J.C.; Tan, D.X.; Sainz, R.M.; Alatorre-Jimenez, M.; Qin, L. Melatonin as an antioxidant: under promises but over delivers. J. Pineal Res., 2016, 61(3), 253-278.
[http://dx.doi.org/10.1111/jpi.12360] [PMID: 27500468]
[35]
Miao, Y.; Chen, Y.; Liu, X.; Diao, J.; Zhao, N.; Shi, X.; Wang, Y. Melatonin decorated 3D-printed beta-tricalcium phosphate scaffolds promoting bone regeneration in a rat calvarial defect model. J. Mater. Chem. B Mater. Biol. Med., 2019, 7(20), 3250-3259.
[http://dx.doi.org/10.1039/C8TB03361G]
[36]
Song, W.; Ma, Z.; Wang, C.; Li, H.; He, Y. Pro-chondrogenic and immunomodulatory melatonin-loaded electrospun membranes for tendon-to-bone healing. J. Mater. Chem. B Mater. Biol. Med., 2019, 7(42), 6564-6575.
[http://dx.doi.org/10.1039/C9TB01516G] [PMID: 31588948]
[37]
Maria, S.; Samsonraj, R.M.; Munmun, F.; Glas, J.; Silvestros, M.; Kotlarczyk, M.P.; Rylands, R.; Dudakovic, A.; van Wijnen, A.J.; Enderby, L.T.; Lassila, H.; Dodda, B.; Davis, V.L.; Balk, J.; Burow, M.; Bunnell, B.A.; Witt-Enderby, P.A. Biological effects of melatonin on osteoblast/osteoclast cocultures, bone, and quality of life: Implications of a role for MT2 melatonin receptors, MEK1/2, and MEK5 in melatonin-mediated osteoblastogenesis. J. Pineal Res., 2018, 64(3)
[http://dx.doi.org/10.1111/jpi.12465] [PMID: 29285799]
[38]
Maria, S.; Swanson, M.H.; Enderby, L.T.; D’Amico, F.; Enderby, B.; Samsonraj, R.M.; Dudakovic, A.; van Wijnen, A.J.; Witt-Enderby, P.A. Melatonin-micronutrients Osteopenia Treatment Study (MOTS): a translational study assessing melatonin, strontium (citrate), vitamin D3 and vitamin K2 (MK7) on bone density, bone marker turnover and health related quality of life in postmenopausal osteopenic women following a one-year double-blind RCT and on osteoblast-osteoclast co-cultures. Aging (Albany NY), 2017, 9(1), 256-285.
[http://dx.doi.org/10.18632/aging.101158] [PMID: 28130552]
[39]
Marsell, R.; Einhorn, T.A. The biology of fracture healing. Injury, 2011, 42(6), 551-555.
[http://dx.doi.org/10.1016/j.injury.2011.03.031] [PMID: 21489527]
[40]
Einhorn, T.A. The cell and molecular biology of fracture healing. Clin. Orthop. Relat. Res., 1998, (355)(Suppl.), S7-S21.
[41]
Khosla, S.; Hofbauer, L.C. Osteoporosis treatment: recent developments and ongoing challenges. Lancet Diabetes Endocrinol., 2017, 5(11), 898-907.
[http://dx.doi.org/10.1016/S2213-8587(17)30188-2] [PMID: 28689769]
[42]
Mullard, A. Merck &Co. drops osteoporosis drug odanacatib. Nat. Rev. Drug Discov., 2016, 15(10), 669-669.
[PMID: 27681784]
[43]
Ettinger, B.; Black, D.M.; Mitlak, B.H.; Knickerbocker, R.K.; Nickelsen, T.; Genant, H.K.; Christiansen, C.; Delmas, P.D.; Zanchetta, J.R.; Stakkestad, J.; Glüer, C.C.; Krueger, K.; Cohen, F.J.; Eckert, S.; Ensrud, K.E.; Avioli, L.V.; Lips, P.; Cummings, S.R. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. JAMA, 1999, 282(7), 637-645.
[http://dx.doi.org/10.1001/jama.282.7.637] [PMID: 10517716]
[44]
Riggs, B.L.; Hartmann, L.C. Selective estrogen-receptor modulators -- mechanisms of action and application to clinical practice. N. Engl. J. Med., 2003, 348(7), 618-629.
[http://dx.doi.org/10.1056/NEJMra022219] [PMID: 12584371]
[45]
Cosman, F.; Crittenden, D.B.; Adachi, J.D.; Binkley, N.; Czerwinski, E.; Ferrari, S.; Hofbauer, L.C.; Lau, E.; Lewiecki, E.M.; Miyauchi, A.; Zerbini, C.A.F.; Milmont, C.E.; Chen, L.; Maddox, J.; Meisner, P.D.; Libanati, C.; Grauer, A. Romosozumab Treatment in postmenopausal women with osteoporosis. N. Engl. J. Med., 2016, 375(16), 1532-1543.
[http://dx.doi.org/10.1056/NEJMoa1607948] [PMID: 27641143]
[46]
Vahle, J.L.; Long, G.G.; Sandusky, G.; Westmore, M.; Ma, Y.L.; Sato, M. Bone neoplasms in F344 rats given teriparatide [rhPTH(1-34)] are dependent on duration of treatment and dose. Toxicol. Pathol., 2004, 32(4), 426-438.
[http://dx.doi.org/10.1080/01926230490462138] [PMID: 15204966]
[47]
Dimitri, P.; Rosen, C. The central nervous system and bone metabolism: An Evolving Story. Calcif. Tissue Int., 2017, 100(5), 476-485.
[http://dx.doi.org/10.1007/s00223-016-0179-6] [PMID: 27501818]
[48]
Lahmar, S.; Kessabi, K.; Banni, M.; Messaoudi, I. First evidence on protective effect of exogenous melatonin supplementation against disruption of the estrogenic pathway in bone metabolism of killifish (Aphanius fasciatus). Fish Physiol. Biochem., 2020, 46(2), 747-757.
[http://dx.doi.org/10.1007/s10695-019-00748-w] [PMID: 31853706]
[49]
Michalowska, M.; Znorko, B.; Kaminski, T.; Oksztulska-Kolanek, E.; Pawlak, D. New insights into tryptophan and its metabolites in the regulation of bone metabolism. J. Physiol. Pharmacol., 2015, 66(6), 779-791.
[PMID: 26769827]
[50]
Stauch, B.; Johansson, L.C.; McCorvy, J.D.; Patel, N.; Han, G.W.; Huang, X.P.; Gati, C.; Batyuk, A.; Slocum, S.T.; Ishchenko, A.; Brehm, W.; White, T.A.; Michaelian, N.; Madsen, C.; Zhu, L.; Grant, T.D.; Grandner, J.M.; Shiriaeva, A.; Olsen, R.H.J.; Tribo, A.R.; Yous, S.; Stevens, R.C.; Weierstall, U.; Katritch, V.; Roth, B.L.; Liu, W.; Cherezov, V. Structural basis of ligand recognition at the human MT1 melatonin receptor. Nature, 2019, 569(7755), 284-288.
[http://dx.doi.org/10.1038/s41586-019-1141-3] [PMID: 31019306]
[51]
Wang, Q; Zhu, D; Ping, S; Li, C; Pang, K; Zhu, S; Zhang, J; Comai, S; Sun, J Melatonin recovers sleep phase delayed by MK- 801 through the melatonin MT(2)receptor- Ca2+-CaMKII-CREB pathway in the ventrolateral preoptic nucleus. J Pineal Res.,
[52]
Radio, N.M.; Doctor, J.S.; Witt-Enderby, P.A. Melatonin enhances alkaline phosphatase activity in differentiating human adult mesenchymal stem cells grown in osteogenic medium in via MT2 melatonin receptors and the MEK/ERK (1/2) signaling cascade. J. Pineal Res., 2006, 40(4), 332-342.
[http://dx.doi.org/10.1111/j.1600-079X.2006.00318.x] [PMID: 16635021]
[53]
Zhou, Y.; Wang, C.; Si, J.; Wang, B.; Zhang, D.; Ding, D.; Zhang, J.; Wang, H. Melatonin up-regulates bone marrow mesenchymal stem cells osteogenic action but suppresses their mediated osteoclastogenesis in via MT2 -inactivated NF-κB pathway. Br. J. Pharmacol., 2020, 177(9), 2106-2122.
[http://dx.doi.org/10.1111/bph.14972] [PMID: 31900938]
[54]
Yim, A.P.; Yeung, H.Y.; Sun, G.; Lee, K.M.; Ng, T.B.; Lam, T.P.; Ng, B.K.; Qiu, Y.; Moreau, A.; Cheng, J.C. Abnormal skeletal growth in adolescent idiopathic scoliosis is associated with abnormal quantitative expression of melatonin receptor, MT2. Int. J. Mol. Sci., 2013, 14(3), 6345-6358.
[http://dx.doi.org/10.1111/jpi.12423] [PMID: 28512916]
[55]
Yim, A.P.; Yeung, H.Y.; Sun, G.; Lee, K.M.; Ng, T.B.; Lam, T.P.; Ng, B.K.; Qiu, Y.; Moreau, A.; Cheng, J.C. Abnormal skeletal growth in adolescent idiopathic scoliosis is associated with abnormal quantitative expression of melatonin receptor, MT2. Int. J. Mol. Sci., 2013, 14(3), 6345-6358.
[http://dx.doi.org/10.3390/ijms14036345] [PMID: 23519105]
[56]
Li, X.; Li, Z.; Wang, J.; Li, Z.; Cui, H.; Dai, G.; Chen, S.; Zhang, M.; Zheng, Z.; Zhan, Z.; Liu, H. Wnt4 signaling mediates protective effects of melatonin on new bone formation in an inflammatory environment. FASEB J., 2019, 33(9), 10126-10139.
[http://dx.doi.org/10.1096/fj.201900093RR] [PMID: 31216173]
[57]
Park, K.H.; Kang, J.W.; Lee, E.M.; Kim, J.S.; Rhee, Y.H.; Kim, M.; Jeong, S.J.; Park, Y.G.; Kim, S.H. Melatonin promotes osteoblastic differentiation through the BMP/ERK/Wnt signaling pathways. J. Pineal Res., 2011, 51(2), 187-194.
[http://dx.doi.org/10.1111/j.1600-079X.2011.00875.x] [PMID: 21470302]
[58]
Son, J.H.; Cho, Y.C.; Sung, I.Y.; Kim, I.R.; Park, B.S.; Kim, Y.D. Melatonin promotes osteoblast differentiation and mineralization of MC3T3-E1 cells under hypoxic conditions through activation of PKD/p38 pathways. J. Pineal Res., 2014, 57(4), 385-392.
[http://dx.doi.org/10.1111/jpi.12177] [PMID: 25250639]
[59]
Zhu, G.; Ma, B.; Dong, P.; Shang, J.; Gu, X.; Zi, Y. Melatonin promotes osteoblastic differentiation and regulates PDGF/AKT signaling pathway. Cell Biol. Int., 2020, 44(2), 402-411.
[http://dx.doi.org/10.1002/cbin.11240] [PMID: 31535749]
[60]
Shuai, Y.; Liao, L.; Su, X.; Yu, Y.; Shao, B.; Jing, H.; Zhang, X.; Deng, Z.; Jin, Y. Melatonin treatment improves mesenchymal stem cells therapy by preserving stemness during long-term in vitro expansion. Theranostics, 2016, 6(11), 1899-1917.
[http://dx.doi.org/10.7150/thno.15412] [PMID: 27570559]
[61]
Knani, L.; Bartolini, D.; Kechiche, S.; Tortoioli, C.; Murdolo, G.; Moretti, M.; Messaoudi, I.; Reiter, R.J.; Galli, F. Melatonin prevents cadmium-induced bone damage: First evidence on an improved osteogenic/adipogenic differentiation balance of mesenchymal stem cells as underlying mechanism. J. Pineal Res., 2019, 67(3)e12597
[http://dx.doi.org/10.1111/jpi.12597] [PMID: 31340072]
[62]
Zhang, L.; Su, P.; Xu, C.; Chen, C.; Liang, A.; Du, K.; Peng, Y.; Huang, D. Melatonin inhibits adipogenesis and enhances osteogenesis of human mesenchymal stem cells by suppressing PPARγ expression and enhancing Runx2 expression. J. Pineal Res., 2010, 49(4), 364-372.
[http://dx.doi.org/10.1111/j.1600-079X.2010.00803.x] [PMID: 20738756]
[63]
Ping, Z.; Hu, X.; Wang, L.; Shi, J.; Tao, Y.; Wu, X.; Hou, Z.; Guo, X.; Zhang, W.; Yang, H.; Xu, Y.; Wang, Z.; Geng, D. Melatonin attenuates titanium particle-induced osteolysis in via activation of Wnt/β-catenin signaling pathway. Acta Biomater., 2017, 51, 513-525.
[http://dx.doi.org/10.1016/j.actbio.2017.01.034] [PMID: 28088671]
[64]
Sanchez-Hidalgo, M.; Lu, Z.; Tan, D.X.; Maldonado, M.D.; Reiter, R.J.; Gregerman, R.I. Melatonin inhibits fatty acid-induced triglyceride accumulation in ROS17/2.8 cells: implications for osteoblast differentiation and osteoporosis. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2007, 292(6), R2208-R2215.
[http://dx.doi.org/10.1152/ajpregu.00013.2007] [PMID: 17379847]
[65]
Yang, F.; Yang, L.; Li, Y.; Yan, G.; Feng, C.; Liu, T.; Gong, R.; Yuan, Y.; Wang, N.; Idiiatullina, E.; Bikkuzin, T.; Pavlov, V.; Li, Y.; Dong, C.; Wang, D.; Cao, Y.; Han, Z.; Zhang, L.; Huang, Q.; Ding, F.; Bi, Z.; Cai, B. Melatonin protects bone marrow mesenchymal stem cells against iron overload-induced aberrant differentiation and senescence. J. Pineal Res., 2017, 63(3)
[http://dx.doi.org/10.1111/jpi.12422] [PMID: 28500782]
[66]
Lian, C.; Wu, Z.; Gao, B.; Peng, Y.; Liang, A.; Xu, C.; Liu, L.; Qiu, X.; Huang, J.; Zhou, H.; Cai, Y.; Su, P.; Huang, D. Melatonin reversed tumor necrosis factor-alpha-inhibited osteogenesis of human mesenchymal stem cells by stabilizing SMAD1 protein. J. Pineal Res., 2016, 61(3), 317-327.
[http://dx.doi.org/10.1111/jpi.12349] [PMID: 27265199]
[67]
Yang, Y.; Fan, C.; Deng, C.; Zhao, L.; Hu, W.; Di, S.; Ma, Z.; Zhang, Y.; Qin, Z.; Jin, Z.; Yan, X.; Jiang, S.; Sun, Y.; Yi, W. Melatonin reverses flow shear stress-induced injury in bone marrow mesenchymal stem cells in via activation of AMP-activated protein kinase signaling. J. Pineal Res., 2016, 60(2), 228-241.
[http://dx.doi.org/10.1111/jpi.12306] [PMID: 26707568]
[68]
Liu, X.; Gong, Y.; Xiong, K.; Ye, Y.; Xiong, Y.; Zhuang, Z.; Luo, Y.; Jiang, Q.; He, F. Melatonin mediates protective effects on inflammatory response induced by interleukin-1 beta in human mesenchymal stem cells. J. Pineal Res., 2013, 55(1), 14-25.
[http://dx.doi.org/10.1111/jpi.12045] [PMID: 23488678]
[69]
Knani, L.; Venditti, M.; Kechiche, S.; Banni, M.; Messaoudi, I.; Minucci, S. Melatonin protects bone against cadmium-induced toxicity in via activation of Wnt/β-catenin signaling pathway. Toxicol. Mech. Methods, 2020, 30(4), 237-245.
[http://dx.doi.org/10.1080/15376516.2019.1701595] [PMID: 31809235]
[70]
Wang, X.; Liang, T.; Zhu, Y.; Qiu, J.; Qiu, X.; Lian, C.; Gao, B.; Peng, Y.; Liang, A.; Zhou, H.; Yang, X.; Liao, Z.; Li, Y.; Xu, C.; Su, P.; Huang, D. Melatonin prevents bone destruction in mice with retinoic acid-induced osteoporosis. Mol. Med., 2019, 25(1), 43.
[http://dx.doi.org/10.1186/s10020-019-0107-0] [PMID: 32082385]
[71]
Wang, X.; Liang, T.; Zhu, Y.; Qiu, J.; Qiu, X.; Lian, C.; Gao, B.; Peng, Y.; Liang, A.; Zhou, H.; Yang, X.; Liao, Z.; Li, Y.; Xu, C.; Su, P.; Huang, D. Melatonin prevents bone destruction in mice with retinoic acid-induced osteoporosis. Mol. Med., 2019, 25(1), 43.
[http://dx.doi.org/10.1186/s10020-019-0107-0]
[72]
Fu, S.; Kuwahara, M.; Uchida, Y.; Koudo, S.; Hayashi, D.; Shimomura, Y.; Takagaki, A.; Nishida, T.; Maruyama, Y.; Ikegame, M.; Hattori, A.; Kubota, S.; Hattori, T. Circadian production of melatonin in cartilage modifies rhythmic gene expression. J. Endocrinol., 2019, 241(2), 161-173.
[http://dx.doi.org/10.1530/JOE-19-0022] [PMID: 30889551]
[73]
Gao, W.; Lin, M.; Liang, A.; Zhang, L.; Chen, C.; Liang, G.; Xu, C.; Peng, Y.; Chen, C.; Huang, D.; Su, P. Melatonin enhances chondrogenic differentiation of human mesenchymal stem cells. J. Pineal Res., 2014, 56(1), 62-70.
[http://dx.doi.org/10.1111/jpi.12098] [PMID: 24117903]
[74]
Wu, Z.; Qiu, X.; Gao, B.; Lian, C.; Peng, Y.; Liang, A.; Xu, C.; Gao, W.; Zhang, L.; Su, P.; Rong, L.; Huang, D. Melatonin-mediated miR-526b-3p and miR-590-5p upregulation promotes chondrogenic differentiation of human mesenchymal stem cells. J. Pineal Res., 2018, 65(1)e12483
[http://dx.doi.org/10.1111/jpi.12483] [PMID: 29498095]
[75]
Gao, B.; Gao, W.; Wu, Z.; Zhou, T.; Qiu, X.; Wang, X.; Lian, C.; Peng, Y.; Liang, A.; Qiu, J.; Zhu, Y.; Xu, C.; Li, Y.; Su, P.; Huang, D. Melatonin rescued interleukin 1 beta-impaired chondrogenesis of human mesenchymal stem cells. Stem Cell Res. Ther., 2018, 9(162)
[76]
Bonnet, N.; Bourgoin, L.; Biver, E.; Douni, E.; Ferrari, S. RANKL inhibition improves muscle strength and insulin sensitivity and restores bone mass. J. Clin. Invest., 2019, 129(8), 3214-3223.
[http://dx.doi.org/10.1172/JCI125915] [PMID: 31120440]
[77]
Takayanagi, H.; Kim, S.; Koga, T.; Nishina, H.; Isshiki, M.; Yoshida, H.; Saiura, A.; Isobe, M.; Yokochi, T.; Inoue, J.; Wagner, E.F.; Mak, T.W.; Kodama, T.; Taniguchi, T. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell, 2002, 3(6), 889-901.
[http://dx.doi.org/10.1016/S1534-5807(02)00369-6] [PMID: 12479813]
[78]
Simonet, W.S.; Lacey, D.L.; Dunstan, C.R.; Kelley, M.; Chang, M.S.; Lüthy, R.; Nguyen, H.Q.; Wooden, S.; Bennett, L.; Boone, T.; Shimamoto, G.; DeRose, M.; Elliott, R.; Colombero, A.; Tan, H.L.; Trail, G.; Sullivan, J.; Davy, E.; Bucay, N.; Renshaw-Gegg, L.; Hughes, T.M.; Hill, D.; Pattison, W.; Campbell, P.; Sander, S.; Van, G.; Tarpley, J.; Derby, P.; Lee, R.; Boyle, W.J. Osteoprotegerin: A novel secreted protein involved in the regulation of bone density. Cell, 1997, 89(2), 309-319.
[http://dx.doi.org/10.1016/S0092-8674(00)80209-3] [PMID: 9108485]
[79]
Ikegame, M.; Hattori, A.; Tabata, M.J.; Kitamura, K.I.; Tabuchi, Y.; Furusawa, Y.; Maruyama, Y.; Yamamoto, T.; Sekiguchi, T.; Matsuoka, R.; Hanmoto, T.; Ikari, T.; Endo, M.; Omori, K.; Nakano, M.; Yashima, S.; Ejiri, S.; Taya, T.; Nakashima, H.; Shimizu, N.; Nakamura, M.; Kondo, T.; Hayakawa, K.; Takasaki, I.; Kaminishi, A.; Akatsuka, R.; Sasayama, Y.; Nishiuchi, T.; Nara, M.; Iseki, H.; Chowdhury, V.S.; Wada, S.; Ijiri, K.; Takeuchi, T.; Suzuki, T.; Ando, H.; Matsuda, K.; Somei, M.; Mishima, H.; Mikuni-Takagaki, Y.; Funahashi, H.; Takahashi, A.; Watanabe, Y.; Maeda, M.; Uchida, H.; Hayashi, A.; Kambegawa, A.; Seki, A.; Yano, S.; Shimazu, T.; Suzuki, H.; Hirayama, J.; Suzuki, N. Melatonin is a potential drug for the prevention of bone loss during space flight. J. Pineal Res., 2019, 67(3)e12594
[http://dx.doi.org/10.1111/jpi.12594] [PMID: 31286565]
[80]
Nakano, M.; Ikegame, M.; Igarashi-Migitaka, J.; Maruyama, Y.; Suzuki, N.; Hattori, A. Suppressive effect of melatonin on osteoclast function in via osteocyte calcitonin. J. Endocrinol., 2019, 242(2), 13-23.
[http://dx.doi.org/10.1530/JOE-18-0707] [PMID: 31042672]
[81]
Kim, H.J.; Kim, H.J.; Bae, M.K.; Kim, Y.D. Suppression of osteoclastogenesis by melatonin: a melatonin receptor-independent action. Int. J. Mol. Sci., 2017, 18(6)E1142
[http://dx.doi.org/10.3390/ijms18061142] [PMID: 28587149]
[82]
Bae, W.J.; Park, J.S.; Kang, S.K.; Kwon, I.K.; Kim, E.C. Effects of melatonin and its underlying mechanism on ethanol-stimulated senescence and osteoclastic differentiation in human periodontal ligament cells and cementoblasts. Int. J. Mol. Sci., 2018, 19(6)E1742
[http://dx.doi.org/10.3390/ijms19061742] [PMID: 29895782]
[83]
Ramírez-Fernández, M.P.; Calvo-Guirado, J.L.; de-Val, J.E.; Delgado-Ruiz, R.A.; Negri, B.; Pardo-Zamora, G.; Peñarrocha, D.; Barona, C.; Granero, J.M.; Alcaraz-Baños, M. Melatonin promotes angiogenesis during repair of bone defects: a radiological and histomorphometric study in rabbit tibiae. Clin. Oral Investig., 2013, 17(1), 147-158.
[http://dx.doi.org/10.1007/s00784-012-0684-6] [PMID: 22323056]
[84]
Yildirimturk, S.; Batu, S.; Alatli, C.; Olgac, V.; Firat, D.; Sirin, Y. The effects of supplemental melatonin administration on the healing of bone defects in streptozotocin-induced diabetic rats. J. Appl. Oral Sci., 2016, 24(3), 239-249.
[http://dx.doi.org/10.1590/1678-775720150570] [PMID: 27383705]
[85]
Lee, J.H.; Han, Y.; Lee, S.H. Potentiation of biological effects of mesenchymal stem cells in ischemic conditions by melatonin in via upregulation of cellular prion protein expression. J. Pineal Res., 2017, 62(2)
[http://dx.doi.org/10.1111/jpi.12385]
[86]
Lee, F.Y.; Sun, C.K.; Sung, P.H.; Chen, K.H.; Chua, S.; Sheu, J.J.; Chung, S.Y.; Chai, H.T.; Chen, Y.L.; Huang, T.H.; Huang, C.R.; Li, Y.C.; Luo, C.W.; Yip, H.K. Daily melatonin protects the endothelial lineage and functional integrity against the aging process, oxidative stress, and toxic environment and restores blood flow in critical limb ischemia area in mice. J. Pineal Res., 2018, 65(2)e12489
[http://dx.doi.org/10.1111/jpi.12489] [PMID: 29570854]
[87]
Carbajo-Pescador, S.; Ordoñez, R.; Benet, M.; Jover, R.; García-Palomo, A.; Mauriz, J.L.; González-Gallego, J. Inhibition of VEGF expression through blockade of Hif1α and STAT3 signalling mediates the anti-angiogenic effect of melatonin in HepG2 liver cancer cells. Br. J. Cancer, 2013, 109(1), 83-91.
[http://dx.doi.org/10.1038/bjc.2013.285] [PMID: 23756865]
[88]
Goradel, N.H.; Asghari, M.H.; Moloudizargari, M.; Negahdari, B.; Haghi-Aminjan, H.; Abdollahi, M. Melatonin as an angiogenesis inhibitor to combat cancer: Mechanistic evidence. Toxicol. Appl. Pharmacol., 2017, 335, 56-63.
[http://dx.doi.org/10.1016/j.taap.2017.09.022] [PMID: 28974455]
[89]
Zonta, Y.R.; Martinez, M.; Camargo, I.C.C.; Domeniconi, R.F.; Lupi Júnior, L.A.; Pinheiro, P.F.F.; Reiter, R.J.; Martinez, F.E.; Chuffa, L.G.A. Melatonin reduces angiogenesis in serous papillary ovarian carcinoma of ethanol-preferring rats. Int. J. Mol. Sci., 2017, 18(4)E763
[http://dx.doi.org/10.3390/ijms18040763] [PMID: 28398226]
[90]
González-González, A.; González, A.; Alonso-González, C.; Menéndez-Menéndez, J.; Martínez-Campa, C.; Cos, S. Complementary actions of melatonin on angiogenic factors, the angiopoietin/Tie2 axis and VEGF, in co cultures of human endothelial and breast cancer cells. Oncol. Rep., 2018, 39(1), 433-441.
[PMID: 29115538]
[91]
Manolagas, S.C. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr. Rev., 2010, 31(3), 266-300.
[http://dx.doi.org/10.1210/er.2009-0024] [PMID: 20051526]
[92]
Aro, H.T.; Alm, J.J.; Moritz, N.; Mäkinen, T.J.; Lankinen, P. Low BMD affects initial stability and delays stem osseointegration in cementless total hip arthroplasty in women: a 2-year RSA study of 39 patients. Acta Orthop., 2012, 83(2), 107-114.
[http://dx.doi.org/10.3109/17453674.2012.678798] [PMID: 22489886]
[93]
Wauquier, F.; Leotoing, L.; Coxam, V.; Guicheux, J.; Wittrant, Y. Oxidative stress in bone remodelling and disease. Trends Mol. Med., 2009, 15(10), 468-477.
[http://dx.doi.org/10.1016/j.molmed.2009.08.004] [PMID: 19811952]
[94]
Lee, N.K.; Choi, Y.G.; Baik, J.Y.; Han, S.Y.; Jeong, D.W.; Bae, Y.S.; Kim, N.; Lee, S.Y. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood, 2005, 106(3), 852-859.
[http://dx.doi.org/10.1182/blood-2004-09-3662] [PMID: 15817678]
[95]
Allegra, M.; Reiter, R.J.; Tan, D.X.; Gentile, C.; Tesoriere, L.; Livrea, M.A. The chemistry of melatonin’s interaction with reactive species. J. Pineal Res., 2003, 34(1), 1-10.
[http://dx.doi.org/10.1034/j.1600-079X.2003.02112.x] [PMID: 12485365]
[96]
melchiorri, D.; sewerynek, E.; poeggeler, B.; barlowwalden, L.; chuang, JI.; acunacastroviejo, D. A review of the evidence supporting melatonins role as an antioxidant. J. Pineal Res., 1995, 18(1), 1-11.
[http://dx.doi.org/10.1111/j.1600-079X.1995.tb00133.x] [PMID: 7776173]
[97]
Zhang, H.M.; Zhang, Y. Melatonin: A well-documented antioxidant with conditional pro-oxidant actions. J. Pineal Res., 2014, 57(2), 131-146.
[http://dx.doi.org/10.1111/jpi.12162] [PMID: 25060102]
[98]
Reiter, R.J. Oxidative processes and antioxidative defense mechanisms in the aging brain. FASEB J., 1995, 9(7), 526-533.
[http://dx.doi.org/10.1096/fasebj.9.7.7737461] [PMID: 7737461]
[99]
Tan, D.; Chen, L.D.; Poeggeler, B.; Manchester, L.C.; Reiter, R. Melatonin: A potent endogenous hydroxyl radical scavenger. Endocr. J., 1993, 1, 57-60.
[100]
Tan, D.X.; Manchester, L.C.; Terron, M.P.; Flores, L.J.; Reiter, R.J. One molecule, many derivatives: A never-ending interaction of melatonin with reactive oxygen and nitrogen species? J. Pineal Res., 2007, 42(1), 28-42.
[http://dx.doi.org/10.1111/j.1600-079X.2006.00407.x] [PMID: 17198536]
[101]
Zhou, W.; Liu, Y.; Shen, J.; Yu, B.; Bai, J.; Lin, J.; Guo, X.; Sun, H.; Chen, Z.; Yang, H.; Xu, Y.; Geng, D. Melatonin Increases Bone Mass around the Prostheses of OVX Rats by Ameliorating Mitochondrial Oxidative Stress in via the SIRT3/SOD2 Signaling Pathway. Oxid. Med. Cell. Longev., 2019, 2019(4019619)4019619
[http://dx.doi.org/10.1155/2019/4019619] [PMID: 31110599]
[102]
Chen, W.; Chen, X.; Chen, A.C.; Shi, Q.; Pan, G.; Pei, M.; Yang, H.; Liu, T.; He, F. Melatonin restores the osteoporosis-impaired osteogenic potential of bone marrow mesenchymal stem cells by preserving SIRT1-mediated intracellular antioxidant properties. Free Radic. Biol. Med., 2020, 146, 92-106.
[http://dx.doi.org/10.1016/j.freeradbiomed.2019.10.412] [PMID: 31669348]
[103]
Zhou, H.; Li, D.; Zhu, P.; Hu, S.; Hu, N.; Ma, S.; Zhang, Y.; Han, T.; Ren, J.; Cao, F.; Chen, Y. Melatonin suppresses platelet activation and function against cardiac ischemia/reperfusion injury in via PPAR gamma/FUNDC1/mitophagy pathways. J. Pineal Res., 2017, 63(e124384)
[104]
Zhou, H.; Ma, Q.; Zhu, P.; Ren, J.; Reiter, R.J.; Chen, Y. Protective role of melatonin in cardiac ischemia-reperfusion injury: From pathogenesis to targeted therapy. J. Pineal Res., 2018, 64(3)
[http://dx.doi.org/10.1111/jpi.12471] [PMID: 29363153]
[105]
Zhang, Y.; Wang, Y.; Xu, J.; Tian, F.; Hu, S.; Chen, Y.; Fu, Z. Melatonin attenuates myocardial ischemia-reperfusion injury in via improving mitochondrial fusion/mitophagy and activating the AMPK-OPA1 signaling pathways. J. Pineal Res., 2019, 66(2)e12542
[http://dx.doi.org/10.1111/jpi.12542] [PMID: 30516280]
[106]
Raygan, F.; Ostadmohammadi, V.; Bahmani, F.; Reiter, R.J.; Asemi, Z. Melatonin administration lowers biomarkers of oxidative stress and cardio-metabolic risk in type 2 diabetic patients with coronary heart disease: A randomized, double-blind, placebo-controlled trial. Clin. Nutr., 2019, 38(1), 191-196.
[http://dx.doi.org/10.1016/j.clnu.2017.12.004] [PMID: 29275919]
[107]
Wang, Z.; Zhou, F.; Dou, Y.; Tian, X.; Liu, C.; Li, H.; Shen, H.; Chen, G. Melatonin allein viates intracerebral hemorrhage-induced secondary brain injury in rats in via suppressing apoptosis, inflammation, oxidative stress, DNA damage, and mitochondria injury. Transl. Stroke Res., 2018, 9(1), 74-91.
[http://dx.doi.org/10.1007/s12975-017-0559-x] [PMID: 28766251]
[108]
Kilic, U.; Caglayan, A.B.; Beker, M.C.; Gunal, M.Y.; Caglayan, B.; Yalcin, E.; Kelestemur, T.; Gundogdu, R.Z.; Yulug, B.; Yılmaz, B.; Kerman, B.E.; Kilic, E. Particular phosphorylation of PI3K/Akt on Thr308 in via PDK-1 and PTEN mediates melatonin’s neuroprotective activity after focal cerebral ischemia in mice. Redox Biol., 2017, 12, 657-665.
[http://dx.doi.org/10.1016/j.redox.2017.04.006] [PMID: 28395173]
[109]
Zheng, Y.; Hou, J.; Liu, J.; Yao, M.; Li, L.; Zhang, B.; Zhu, H.; Wang, Z. Inhibition of autophagy contributes to melatonin-mediated neuroprotection against transient focal cerebral ischemia in rats. J. Pharmacol. Sci., 2014, 124(3), 354-364.
[http://dx.doi.org/10.1254/jphs.13220FP] [PMID: 24646622]
[110]
Bhattacharya, P.; Pandey, A.K.; Paul, S.; Patnaik, R. Melatonin renders neuroprotection by protein kinase C mediated aquaporin-4 inhibition in animal model of focal cerebral ischemia. Life Sci., 2014, 100(2), 97-109.
[http://dx.doi.org/10.1016/j.lfs.2014.01.085] [PMID: 24530291]
[111]
Galano, A.; Reiter, R.J. Melatonin and its metabolites vs oxidative stress: From individual actions to collective protection. J. Pineal Res., 2018, 65(1)e12514
[http://dx.doi.org/10.1111/jpi.12514] [PMID: 29888508]
[112]
Reiter, R.J. Oxidative damage in the central nervous system: Protection by melatonin. Prog. Neurobiol., 1998, 56(3), 359-384.
[http://dx.doi.org/10.1016/S0301-0082(98)00052-5] [PMID: 9770244]
[113]
Hardeland, R. Antioxidative protection by melatonin: Multiplicity of mechanisms from radical detoxification to radical avoidance. Endocrine, 2005, 27(2), 119-130.
[http://dx.doi.org/10.1385/ENDO:27:2:119] [PMID: 16217125]
[114]
Galano, A.; Tan, D.X.; Reiter, R.J. On the free radical scavenging activities of melatonin’s metabolites, AFMK and AMK. J. Pineal Res., 2013, 54(3), 245-257.
[http://dx.doi.org/10.1111/jpi.12010] [PMID: 22998574]
[115]
Lai, M.; Jin, Z.; Tang, Q.; Lu, M. Sustained release of melatonin from TiO2 nanotubes for modulating osteogenic differentiation of mesenchymal stem cells in vitro. J. Biomater. Sci. Polym. Ed., 2017, 28(15), 1651-1664.
[http://dx.doi.org/10.1080/09205063.2017.1342334] [PMID: 28604249]
[116]
Zhang, L.; Zhang, J.; Ling, Y.; Chen, C.; Liang, A.; Peng, Y.; Chang, H.; Su, P.; Huang, D. Sustained release of melatonin from poly (lactic-co-glycolic acid) (PLGA) microspheres to induce osteogenesis of human mesenchymal stem cells in vitro. J. Pineal Res., 2013, 54(1), 24-32.
[http://dx.doi.org/10.1111/j.1600-079X.2012.01016.x] [PMID: 22712496]
[117]
Gurler, E.B.; Ergul, N.M.; Ozbek, B.; Ekren, N.; Oktar, F.N.; Haskoylu, M.E.; Oner, E.T.; Eroglu, M.S.; Ozbeyli, D.; Korkut, V.; Temiz, A.F.; Kocanalı, N.; Gungordu, R.J.; Kılıckan, D.B.; Gunduz, O. Encapsulated melatonin in polycaprolactone (PCL) microparticles as a promising graft material. Mater. Sci. Eng. C, 2019, 100, 798-808.
[http://dx.doi.org/10.1016/j.msec.2019.03.051] [PMID: 30948117]
[118]
Liu, X.; Chen, Y.; Mao, A.S.; Xuan, C.; Wang, Z.; Gao, H.; An, G.; Zhu, Y.; Shi, X.; Mao, C. Molecular recognition-directed site-specific release of stem cell differentiation inducers for enhanced joint repair. Biomaterials, 2020, 232(119644)119644
[http://dx.doi.org/10.1016/j.biomaterials.2019.119644] [PMID: 31884017]
[119]
Sola-Ruiz, M.F.; Perez-Martinez, C.; Labaig-Rueda, C.; Carda, C.; Martín De Llano, J.J. Behavior of human osteoblast cells cultured on titanium discs in relation to surface roughness and presence of melatonin. Int. J. Mol. Sci., 2017, 18(4)E823
[http://dx.doi.org/10.3390/ijms18040823] [PMID: 28406458]
[120]
Clafshenkel, W.P.; Rutkowski, J.L.; Palchesko, R.N.; Romeo, J.D.; McGowan, K.A.; Gawalt, E.S.; Witt-Enderby, P.A. A novel calcium aluminate-melatonin scaffold enhances bone regeneration within a calvarial defect. J. Pineal Res., 2012, 53(2), 206-218.
[http://dx.doi.org/10.1111/j.1600-079X.2012.00989.x] [PMID: 22462771]
[121]
Altindal, D.C.; James, E.N.; Kaplan, D.L.; Gumusderelioglu, M. Melatonin-induced osteogenesis with methanol-annealed silk materials. J. Bioact. Compat. Polym., 2019, 34(3), 291-305.
[http://dx.doi.org/10.1177/0883911519847489]
[122]
Loi, F.; Córdova, L.A.; Pajarinen, J.; Lin, T.H.; Yao, Z.; Goodman, S.B. Inflammation, fracture and bone repair. Bone, 2016, 86, 119-130.
[http://dx.doi.org/10.1016/j.bone.2016.02.020] [PMID: 26946132]
[123]
Calvo-Guirado, J.L.; Aguilar Salvatierra, A.; Gargallo-Albiol, J.; Delgado-Ruiz, R.A.; Maté Sanchez, J.E.; Satorres-Nieto, M. Zirconia with laser-modified microgrooved surface vs. titanium implants covered with melatonin stimulates bone formation. Experimental study in tibia rabbits. Clin. Oral Implants Res., 2015, 26(12), 1421-1429.
[http://dx.doi.org/10.1111/clr.12472] [PMID: 25155996]
[124]
Willie, B.M.; Petersen, A.; Schmidt-Bleek, K.; Cipitria, A.; Mehta, M.; Strube, P.; Lienau, J.; Wildemann, B.; Fratzl, P.; Duda, G. Designing biomimetic scaffolds for bone regeneration: why aim for a copy of mature tissue properties if nature uses a different approach? Soft Matter, 2010, 6(20), 4976.
[http://dx.doi.org/10.1039/c0sm00262c]
[125]
Goodman, S.B.; Ma, T.; Chiu, R.; Ramachandran, R.; Smith, R.L. Effects of orthopaedic wear particles on osteoprogenitor cells. Biomaterials, 2006, 27(36), 6096-6101.
[http://dx.doi.org/10.1016/j.biomaterials.2006.08.023] [PMID: 16949151]
[126]
Ping, Z.; Wang, Z.; Shi, J.; Wang, L.; Guo, X.; Zhou, W.; Hu, X.; Wu, X.; Liu, Y.; Zhang, W.; Yang, H.; Xu, Y.; Gu, Y.; Geng, D. Inhibitory effects of melatonin on titanium particle-induced inflammatory bone resorption and osteoclastogenesis in via suppression of NF-κB signaling. Acta Biomater., 2017, 62, 362-371.
[http://dx.doi.org/10.1016/j.actbio.2017.08.046] [PMID: 28867647]

Rights & Permissions Print Cite
Article Metrics
39
2
1
1
© 2024 Bentham Science Publishers | Privacy Policy